dietary influences on the development of sucrose acceptability in rats

Dietary Influences on the Development of Sucrose Acceptability in Rats

MARY BERTINO FRANCINE WEHMER

Department of Psycho logy Wayne State University

Detroit, Michigan

Weanling rats were placed on a high-fat diet or chuw. Beginning at 5 weeks of age, they were tested for acceptability of4 sucrose solutions of different concentrations once a week until they showed the previously established adult pattern of acceptability. Subjects on the chow diet showed a gradual transition from a juvenile to adult pattern of acceptability, that is, a progressive downward shift in the concentration of solution that is most acceptable. Subjects on the high-fat diets never showed the adult pattern but continued to display a juvenile pattern of acceptability throughout the experiment. The data obtained from the subjects on the high-fat diets are similar to those on taste preferences in obese humans.

Studies of ingestive responses to differing concentrations of sugar solutions have revealed differences in behavior that are dependent upon the subjects’ ages. Infants and preadolescent children of normal body weight show a sucrose preference that is positively correlated with concentration: the sweeter the solutions, the more they are preferred (Desor, Maller, & Greene, 1977; Grinker, Price, & Greenwood, 1976). Adolescents prefer higher concentrations of sweet solutions than adults (Desor et al., 1977). Like the human infant, 10-day-old rats show stronger appetitive responses to highly concentrated sugar solutions than to less concentrated solutions (Jacobs, Smutz, & DuBose, 1977). By adulthood, however, rats show peak acceptability of sweet solutions at lower concentrations (Ernits & Corbit, 1973).

In man, differences in response to sweet solutions appear to depend, also, on whether the subject was obese or not at the time oftesting. High-birth-weight neonates drink disproportionately more of a sweetened formula than lower-birth-weight infants (Nisbett & Gurwitz, 1970). However, some researchers have found an aversion to concentrated sugar solutions in obese children and adults. The degree of aversion in obese adolescents is positively related to the age of obesity onset. The earlier the onset, the less the preference for the sweeter solutions (Grinker et al., 1976). Others have not found a difference in sweet preferences between obese and normal individuals, but rather a heightened responsiveness (i.e. greater consumption) in the obese to these preferences (Rodin, 1977).

This lack of consistency in the data on sweetness preferences of obese humans is not surprising, in that many factors influencing taste preferences in humans are

Reprint requests should be sent to Francine Wehmer, Department of Psychology, Wayne State University, Detroit, Michigan, 48202, U.S.A.

Received for publication 5 February 1979 Revised for publication 3 December 1979 Developmental Psj%chobiology, 14( 1): 19-28 (1981) 01981 by John Wiley & Sons. Inc.

20 BERTINO AND WEHMER

difficult t o control. Dietary factors appear t o be among them. Weight reduction among the obese appears to produce an increased liking for sweeter solutions (Grinker et al., 1976). A similar effect is seen in rats in that food deprivation resulting in weight reduction increases the amount of sucrose solution consumed (Collier & Hirsch, 1977). Early studies by Richter and Schmidt (1941) showed that the amount of fat in the diet will influence the amount of sucrose in solution that is ingested, with increases in dietary fat associated with decreases in consumption. Thus, both age and diet appear t o affect sucrose consumption. Inconsistencies reported in studies that utilize human subjects may in part reflect difficulties in controlling the longer-term dietary habits associated with obesity. The aim of this study was to investigate the development of sucrose acceptability in normal rats and compare this with the development of sucrose acceptability in rats on a high-fat diet.

Method

The subjects were 46 female and 30 male Sprague-Dawley albino rats (Rattus norvegicus) obtained at 22 days of age from Spartan Research Laboratories (Haslett, Mich.). They were housed individually in stainless steel cages in a colony room maintained on a 12-hour light: 12-hour dark diurnal cycle. Half of each gender were assigned to the experimental diet. The control subjects were placed on Purina Rodent Laboratory Chow 5001 (23% protein, 5% fat; 4.25 kcal/g). The experimental females were placed on a diet that contained 30% fat, 21% protein, and 37% carbohydrate by weight. The caloric content was 5.50 kcal/g. The experimental males were placed on a diet that contained 36% fat, 19% protein, and 34% carbohydrate. The caloric content was 5.80 kcal/g (Table 1). The experimental diets were fortified with vitamins (Vitamin Fortification Mixture, Nutritional Biochemicals).

When the subjects were 4 weeks of age they were pretrained for 4-5 days to drink a .01M saccharin solution during a 1-hr test period. Formal testing began when the subjects were 5 weeks old. Each day’s testing began at approximately 1230 hours. Food was removed from the cage 1 hr before the test. The water bottle remained in the cage during that hour so that the subjects could satisfy residual postprandial water needs. After the I-hr period, the water bottle was replaced with a bottle containing a sucrose solution. The amount of sucrose consumed during the I-hr test was recorded at which time food and water were returned t o the cage. This schedule insured continuous exposure to fluid, minimizing the possibility that water deprivation contributed to the consumption of the sucrose solution. The presence of food ad

TABLE I . Diet Composition.

Female Male

Purina laboratory chow 53.2% 49.0% Vitamin-free casein x.59f 7.8% Sucrose 10.6% 9.7% Hydrogenated vegeta hle sh ortening 27.6% 33.3% Caloric density 5.5 kca l /g 5.8 kcalig

“Percents a r e by weight. Both diets were supplemented with vitamin fortification mixture (Nutri t ional Biochemicals).

SUCROSE ACCEPTABILITY IN DEVELOPING RATS 21

500 -

400 .

300 . 5 s3 8 r

200 -

100 .

libitum for 22 of the 24 hr minimized the role of food deprivation in the sucrose solution consumed, given the fact that food was removed during the light cycle when rats were not frequently observed eating.

The subjects were exposed to 1 of 4 sucrose solutions of differing concentration at room temperature: .025, .15, .3, and .5 M. These 4 molarities were selected from the adult sucrose acceptability curves developed by Ernits and Corbit (1973) which show that peak sucrose acceptability is obtained in the adult male rat when the concentration is .15M. The remaining 3 molarities represent points that are of less acceptability. Each subject was tested with each solution, 1 molarity per day, with each subject receiving a more concentrated solution on each successive day of the test. Each 4-day test period was followed by 3 days without testing. This completed a weekly test block. The identical test continued until both genders showed the adult acceptability pattern of maximum response to .15Mfor 2 successive test periods. Body weights were taken once a week after the completion of the 1st daily test that week.

Results

Body Weight

By I 1 weeks of age the experimental females weighed significantly more than controls. In contrast, the experimental males weighed significantly less than the controls as early as 6 weeks of age and remained comparatively lighter in weight until they were 12 weeks old (Fig. 1).

I = . .1

3 4 5 6 7 8 9 1 0 1 1 1 2 1 3 1 4

AGE (weeks)

Fig. I . Female and male body weight as a function of age. Sucrose testing began at 5 weeks of age. -.Chow. ---High-fat.


Sucrose Consumpt ion

Because the genders required different numbers of weeks to reach the adult pattern, separate analyses of variance were performed on each gender. The factors analyzed were Diet, Sucrose Molarity, and Age. For each gender, each factor and its associated interactions were significant beyond the .01 level (Table 2). Inspection of rhe data revealed that at 6 weeks of age and thereafter, almost no overlap occurred between the diet groups. Subjects within each diet group, regardless of gender, showed the same developmental stages in their response t o sucrose solutions (Figs. 2 and 3).

Development in t h e Con t ro l s

Stage 1 (Juvenile). At the earliest ages tested, male and female controls showed increasing consumption in response t o increasing concentrations of sucrose. In the female controls, this stage lasted up to 6 weeks of age, whereas in the males, the juvenile stage continued up to 8 weeks of age.

Stage 2 (Transition). During this period, concentrations of sucrose up to .3M continued to stimulate increasingly greater consumption. The highest concentration, .5M, either did not reliably increase further consumption or produced a slight decrease in intake compared to the .3M solutions. In the female, the transition phase occurred between 7 and 10 weeks of age. In the male, the transition stage lasted between weeks 8 and 11.

Stage 3 (Aduft). The previously reported adult pattern of peak acceptability to sucrose in solutions o f . ISM appeared in the females when they were I 1 weeks of age and in the males when they were 12 weeks of age. Concentrations higher o r lower than . I5M were associated with comparatively less consumption.

Development in t h e Experimentals

The experimental diet had 3 major effects on the development of response to sucrose solutions: (1) The experimentals drank, on the average, only 40% of the

TABLE 2. Sucrose Accel,tahilitp-Anal.~ses of Variance.

Source of variation Clf F P

Diet 1/44 96.07 <.01 Age 71308 72.60 <.01 Molarity 31 132 158.65 <.01 Diet X Age 71308 29.45 <.01 Diet X Molarity 31132 16.94 <.01 Age X Molarity 21/924 3.94 <.01 Diet X Age X Molarity 21/924 6.68 <.01

Fema1r.s

Males

Diet I /28 Age 9!252 Molarity 3 /84 Diet X Age 91252

Age X Molarity 27/756 Diet X Age X Molarity 27/756

Diet X Molarity 3 /84

73.70 <.01 81.52 <.01 69.75 <.01 22.52 <.01

8.94 <.01 5.26 <.01 4.89 < . O l


w \

I

\ \

N d

h

W

m

3 X U N I NOILfl'IOS


sucrose consumed by the controls. (2) The experimentals showed relatively less change over weeks in the amount of sucrose they consumed per week. The controls increased sucrose consumption 300% from Week 5 to Week 12. In contrast, the experimentals increased their consumption by only 134% during this same time period. (3) The shapes of the experimental curves were quite different from the shapes of the control curves. Overall, the experimentals appeared to remain in the juvenile stage throughout the experiment, showing peak acceptability to .5M of sucrose solution. However, during the 1st 4 weeks of testing in the females, the curves across molarities were relatively flat, compared to the juvenile period in the controls.

Gender Differences

The factor of Gender was added to the analysis of variance. This required that Week 13 in the males be dropped from the data. No main effect of Gender was identified on sucrose consumption ( F = 2.22, df = 1/72. p > .05). In addition, no interaction appeared between Gender and responsivity to differing molarities of sucrose ( F = 1.05, df = 31216.p > .05). A significant interaction between Gender and Age(F= 12.55. df=7/504,p< .Ol)reflectedthefact that older(Weeks 10-12)females drank significantly less sucrose per week than comparable males. A significant Gender X Diet XAgeinteraction(F= 5.03, df=7/504,p<.Ol)revealed thattheGenderXAge interaction was almost entirely restricted to controls. No difference appeared in the amount of sucrose consumed by 10- and 11-week-old males and females on the high-fat diet. During Week 12, however, the females on the high-fat diet drank significantly less than the males on high-fat diet 0, < .05).

A significant Gender X Age X Molarity interaction (F= 3.50, df= 2 1 / 504,p < .01) revealed that the females and males changed their responses to differing molarities of solution at different ages. This was described in the section on developmental stages above. There was also a significant, though uninterpretable, 4-way interaction between sex, age, diet, and molarity.

Discussion

In this study, we found that young rats show systematic change during development in the way they respond to sweet solutions. The change can be categorized into 3 developmental stages: Stage I (Juvenile) appears to last until the rats are 6-8 weeks old, with females leaving this stage at an earlier age (6 weeks) than males (8 weeks). During this stage, rats consume very sweet solutions more readily than those of lower concentrations. Stage 2 (Transition) lasts until the animals are 10-1 1 weeks old, depending on gender. In this stage, acceptability of the highest sucrose concentration starts to drop relative to the intake pattern of the other 3 concentrations. In Stage 3 (Adult), acceptability of sucrose peaks at a lower concentration (. 15M), with relative aversion shown to the 2 sweeter solutions. This last stage has been reported previously as the norm for adult male rats when this testing procedure is employed (Ernits & Corbit, 1973).

Our results compare favorably with data collected on the preference and acceptability behavior of humans in regard to sweet tastes. Human infants show greater acceptability of sweet solutions of higher concentrations, consuming more of .3M than .2M glucose solutions (Desor et al., 1977). Whether this trend in increasing acceptability continues with even higher concentrations of sweet solutions, as happened with our rats, is not known. Human adolescents show varied behavior with approximately half of those tested showing peak preferences at the highest concentra-

26 BERTINO A N D WEHMER

tions of sucrose (.6M), whereas adults display a relative aversion to this concentration of sucrose with approximately 3 / 4 of the subjects tested preferring sucrose concentrations at or below .3M (Desor et al., 1977). In the adult rat and human, then, the sweetest concentration is no longer the most preferred.

One possible explanation for the developmental difference is that the growing rat may be a hungry rat. In the infant rat with a high growth rate, the more milk that is available, the more it will consume. This hyperphagia continues after weaning, possibly because of the demands for increased thermoregulation and energy expenditure for locomotion, along with those of growth (Kennedy, 1977). If the growing rat is a hungry one, then it may have response patterns t o taste stimuli similar to that of a hungry adult. Sweet preferences in both hungry adult rats and growing rats d o not show the relative aversion toward high concentrations of sweet tastes that is observed in the sated adult (Bacon, Snyder, & Hulse, 1952). Research with other species also suggests there is an increasing response to sweet solutions as a function of hunger (Dethier & Bodenstein, 1958).

In some respects, our subjects on the high-fat diets showed striking similarities to the taste responsivity of obese humans. The experimental rats displayed sucrose intake functions similar to hedonic functions (ratings of pleasantness) obtained from obese humans. In human subjects the perceived pleasantness of sweet solutions does not decrease with satiety as it does in normals (Cabanac & Duclaux, 1970). Instead, in some obese individuals, hedonic value is an increasing function of the level of sucrose concentration (Rodin, Moskowitz, & Bray, 1976). This pattern of response is similar to the pattern of response in hungry humans and rats. The similarity in preference pattern between our experimental subjects and obese humans may suggest that much of the taste responsivity in the obese is an effect of the type of diet they are consuming.

Over time, our controls showed a gradual shift in acceptability from .5M t o . I5M. This shift may have been, in part, a function of the repeated test procedure which was employed. Adult rats that have continuous free access to 2 glucose solutions of different concentrations will initially prefer the high-glucose concentrations. How- ever, after a few days of exposure to these solutions they will shift in preference, consuming more of the initially nonpreferred solutions (Booth, Lovett, & McSheary, 1972). Preference shift has been interpreted as an effect of association between the taste of the solution and longer-term postingestional factors which are maximized when the rat has continuous access to the 2 solutions. Although a learning component may exist in our developmental curves, a substantial component may also be due to the maturation of the rats. This is supported by the fact that the adult curves obtained by Ernits and Corbit (1973) were obtained with little experience, that is, 1 prior exposure to each test solution.

Several possible mechanisms may underlie the developmental changes in the pattern of sucrose acceptability. In tests of brief exposure to sweet solutions, which minimize postingestional effects, adult rats show an acceptability curve similar to that of our young rats (Davis & Levine, 1977). Possibly, the developmental shift in the sucrose acceptability curves was due to changes in postingestional cues or changes in response to postingestional cues to sweet solutions in growing rats. One source of differences in postingestional cues may have been the relatively low volume of solution the young rats were ingesting. A lowered solution intake may not have produced postingestional cues sufficient t o inhibit intake at high concentrations. This same argument may also apply to the subjects on the high-fat diet.

The developmental shift in the displayed sucrose acceptability of the control subjects may have been due to maturational changes in their receptor population.


Changes in anatomical distribution of taste receptors have been shown to occur during postnatal development in rats (Henderson & Smith, 1977). However, the pattern of anatomical change does not match the pattern of taste acceptability shift displayed. Taste receptor populations increase in 2 phases, one ending at 10 days of age and the other at .30 days of age. After 30 days, the receptor population remains relatively constant in number (Henderson & Smith, 1977). This does not match the changes in pattern for taste acceptability in the controls which began at 7 or 8 weeks of age.

Overall sucrose consumption by the subjects on the high-fat diets was low. This may be the result of 2 effects working in the same direction. First, sucrose was present in the diets of the high-fat subjects (9.85% by weight for the males; 10.6% for the females). This may have depressed the subjects’ sucrose intake from the test solutions. Second, animals on high-fat diets in general consume less water than animals on chow diets although they retain the same water intake-to-food intake ratio as subjects on chow diets (Young, Nance, Dwight, & Gorski, 1978).

The absence of the expected gender differences in response to the sucrose solutions was surprising in that others have found that female rats consume more of sweet solutions than male rats (Nance, Gorski, & Panksepp, 1976; Valenstein, Kakolewski, &Cox, 1967; Wade & Zucker, 1969a,b; Zucker, 1969). Our study differed from these studies in that we used a bottle test with 1-hr access instead of a 2-bottle test with continuous access. Possibly, gender differences in intake are expressed only in continuous access preference tests. The lack of gender difference in our experimental paradigm as compared to other paradigms may suggest that gender differences in response to sweet solutions is a longer-term response more sensitive to postingestional factors not evident in shorter-term tests where taste may be a more important factor determining intake. However, because females also show increased intake of nonnutritive saccharin solutions (Wade & Zucker, 1969a), taste factors may be observable only when access to these solutions is for durations longer than 1 hr.

Finally, attention should be drawn to the fact that over time the male subjects on the experimental diet increased their body weights t o a lesser degree than the male subjects on the chow diet, whereas the female subjects on the experimental diet showed increased growth compared to female controls. This gender difference in response to the high-fat diet appeared at the time gender differences in body weight were emerging. We think this is due to the protein content of the diets. The percent protein in the 2 diets was roughly equivalent. However, if the animals eat less of the high-fat diet than they d o of the chow diet, then their absolute daily protein intake may be too low. We have found that animals on a high-fat diet eat less than animals on a chow diet, resulting in a significantly lower protein intake per day (unpublished observations). The observed gender difference in growth as a function of diet may have reflected the fact that the total protein intake in the smaller experimental females was sufficient t o allow growth and even promote obesity, whereas the larger experimental males did not take in sufficient protein during the growth period.

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dietary influences on the development of sucrose acceptability in rats

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